Title: Prior heat waves improve survival of field but not domesticated populations of tobacco hornworm exposed to repeated bacterial infections
Abstract In insects and other invertebrates, prior pathogen exposures can improve immune responses and survival to subsequent infections through immune priming. Alternatively, stress and metabolic costs of multiple infections can impair host immunity and survival. The effects of high‐temperature extremes on host–pathogen interactions are not well understood despite the increasing occurrence of heat waves caused by climate change.The response of insects to heat waves and pathogens depends on recent evolutionary history with selective pressures. Domestication of insect pests has occurred in lab colonies of model species, reducing selective pressures for immune and heat stress responses. Lab strains are often used in immunological or heat stress experiments to represent wild field strains, but the efficacy of this approach is seldom evaluated.Using the tobacco hornworm (Manduca sexta), we tested the impact of a heat wave during initial pathogen exposure on survival of a secondary infection withBacillus thuringiensisbacteria. We used a domesticated lab population and a naturally occurring field population ofM. sextato evaluate the impacts of recent domestication on immune and thermal responses.A heat wave during initial infection significantly increased survival of the secondaryB. thuringiensisinfection in the field, but not the lab population ofM. sexta.In the field population, survival of the repeated infection was temperature dependent: exposure to an initial infection event reduced survival of the secondary infection at the control temperature regime, consistent with a stress effect. However, a heat wave during the initial infection event increased survival of the secondary infection, consistent with immune priming effects.The results of this study demonstrate that (a) insect response to thermal stress and pathogens can depend on recent domestication and (b) responses of hosts to repeat pathogen exposures can be temperature‐dependent, suggesting that cross‐talk between the heat stress and immune memory pathways may have important consequences for host–pathogen outcomes under heat wave events. Read the freePlain Language Summaryfor this article on the Journal blog.  more » « less
Award ID(s):
2029156
PAR ID:
10630502
Author(s) / Creator(s):
; ;
Publisher / Repository:
British Ecological Society
Date Published:
Journal Name:
Functional Ecology
Volume:
39
Issue:
3
ISSN:
0269-8463
Page Range / eLocation ID:
711 to 722
Format(s):
Medium: X
Sponsoring Org:
National Science Foundation
More Like this
  1. Garsin, Danielle A. (Ed.)
    Innate immune priming increases an organism’s survival of a second infection after an initial, non-lethal infection. We usedDrosophila melanogasterand an insect-derived strain ofEnterococcus faecalisto study transcriptional control of priming. In contrast to other pathogens, the enhanced survival in primed animals does not correlate with decreasedE.faecalisload. Further analysis shows that primed organisms tolerate, rather than resist infection. Using RNA-seq of immune tissues, we found many genes were upregulated in only primed flies, suggesting a distinct transcriptional program in response to initial and secondary infections. In contrast, few genes continuously express throughout the experiment or more efficiently re-activate upon reinfection. Priming experiments in immune deficient mutants revealed Imd is largely dispensable for responding to a single infection but needed to fully prime. Together, this indicates the fly’s innate immune response is plastic—differing in immune strategy, transcriptional program, and pathway use depending on infection history. 
    more » « less
  2. Abstract We studied the potential of combining insect immune priming with the introduction of diverse migrants to safeguard individuals from an inbred population from disease as a technique for enhancing genetic rescue efforts.Immune priming in insects refers to the stronger immune response insects have against pathogens following exposure. This enhanced immunity can be passed on to offspring and holds promise for insect conservation efforts against diseases.We compared the fitness benefits to individuals from a small, inbred population of two treatments: the addition of genetically diverse migrants that had not been primed and the addition of immune‐primed migrants. While both types of migrants enhanced reproduction, as in cases of genetic rescue, only primed migrants led to improved survival on exposure to a pathogen.Better immunity led to a trade‐off with reproduction in immune‐primed migrants, but this was not evident upon outcrossing with the target individuals, revealing synergies between hybrid vigour and immune priming.Given the demographic constraints and stochasticity that can exacerbate the effects of disease outbreaks in small populations, our results serve as a proof of concept for combining immune priming with assisted migration, which offers a proactive strategy to mitigate disease impacts while enhancing genetic diversity. 
    more » « less
  3. Abstract Host competence—the ability to acquire, harbour and transmit infections—drives pathogen spread and persistence in multi‐host communities. Evaluating species‐specific competence is critical for predicting transmission, particularly for generalist fungal pathogens likeBatrachochytrium dendrobatidis(Bd). Despite its central role in disease dynamics, we lack an epidemiologically grounded competence metric that rigorously accounts for how infection intensity affects a host's competence. This knowledge gap limits our ability to compare mechanisms across species and assess their roles in pathogen persistence. To address these challenges, we developed a novel, load‐dependent competence metric using host–pathogen Integral Projection Models (IPMs) that integrates variation in susceptibility, within‐host pathogen growth and pathogen shedding dynamics.We applied this metric to laboratory‐based challenge experiments with three common North American amphibians (Notophthalmus viridescens,Rana clamitansandRana catesbeianus) that persist endemically with Bd. Using dose–response assays and repeated pathogen shedding measurements across species, we asked: (i) is there a consistent, non‐linear relationship between infection intensity and pathogen shedding across species? and (ii) which load‐based traits best predict host competence? We quantified four of five components of host competence—susceptibility, pathogen growth, pathogen survival and load‐dependent shedding—and used these to parameterize species‐specific IPMs, integrating competence into a single relative metric across species.We found that Bd shedding increased non‐linearly with infection intensity, contradicting the standard assumption that Bd shedding is linearly related to infection intensity.Notophthalmus viridescensandR. catesbeianuswere the most competent hosts but through distinct pathways: high susceptibility inN. viridescensand elevated shedding rates inR. catesbeianus. In contrast, density‐dependent reductions in pathogen growth and shedding limitedR. clamitanscompetence. Thus, species‐level competence is not determined by a single trait, but emerges from interactions among multiple load‐based processes.Our results demonstrate that variation in competence emerges from distinct, species‐specific processes across multiple dimensions of competence. By linking individual infection dynamics to population‐level transmission potential, our integrative framework provides a more mechanistic approach to predicting host contributions to community‐level pathogen persistence. Read the freePlain Language Summaryfor this article on the Journal blog. 
    more » « less
  4. Abstract Plants have unique chemical and physical traits that can reduce infections in animals ranging from primates to caterpillars. Sunflowers (Helianthus annuus; Asteraceae) are one striking example, with pollen that suppresses infections by the trypanosomatid gut pathogenCrithidia bombiin the common eastern bumble bee (Bombus impatiens). However, the mechanism underlying this effect has remained elusive, and we do not know whether pollens from other Asteraceae species have similar effects.We evaluated whether mechanisms mediating sunflower pollen's antipathogenic effects are physical (due to its spiny exine), chemical (due to metabolites) or both. We also evaluated the degree to which pollen from seven other Asteraceae species reducedC. bombiinfection relative to pollen from sunflower and two non‐Asteraceae species, and whether pollen spine length predicted pathogen suppression.We found that sunflower exines alone reduced infection as effectively as whole sunflower pollen, while sunflower pollen metabolites did not. Furthermore, bees fed pollen from four of seven other Asteraceae had 62%–92% lowerC. bombiinfections than those fed non‐Asteraceae pollen. Spine length, however, did not explain variation in bumble bee infection.Our study indicates that sunflower pollen's capacity to suppressC. bombiis driven by its spiny exine, and that this phenomenon extends to several other Asteraceae species. Our results indicate that sunflower pollen exines are as effective as whole pollen in reducing infection, suggesting that future studies should expand to assess the effects of other species with spiny pollen on pollinator–pathogen dynamics. Read the freePlain Language Summaryfor this article on the Journal blog. 
    more » « less
  5. Synopsis Existing and emerging diseases threaten wildlife populations worldwide and population resilience in the face of disease depends on immune responses. To apply conservation strategies to populations threatened by disease, it is critical to know not only how individuals will respond to the initial exposure of the pathogen but also to determine risks when the pathogen becomes endemic or is reintroduced. Immune responses following a subsequent exposure to a pathogen may vary from initial responses due to several immunological memory mechanisms such as adaptive immune function and innate immune priming/training and tolerance. Alternatively, immune responses may vary as a consequence of resource limitation. Regardless of outcome, these altered responses could impact how individuals respond to successive pathogen exposures in their environment. Disease threatens reptiles worldwide but research on reptilian immunology has lagged behind other taxonomic groups, resulting in large gaps in our understanding of both mechanistic and functional immune responses. Reptiles possess traditionally considered “innate” and “adaptive” immune components, but current literature seems to agree that reptiles depend largely on innate immune components as adaptive responses are slow. We present an exploratory study in which we measured functional immune responses in male red-eared slider turtles (Trachemys scripta elegans) to 2 antigen injections representing bacterial (lipopolysaccharide), viral (polyinosinic-polycytidylic acid; poly(I:C), fungal infections (zymosan), and control (saline), administered 2 weeks apart. We separated serum and buffy layer (serum + BL) from blood samples and manipulated the serum + BL (fresh, frozen, frozen + heat) to systematically inactivate immune components. We conducted microbial killing assays using the manipulated serum + BL with Gram-negative Escherichia coli, Gram-positive Staphylococcus aureus, and the diploid yeast Candida albicans, which allowed us to examine immune responses across various contexts. Although sample sizes were small, we observed varied responses across treatments and serum + BL/microbe assay combinations, suggesting that several mechanisms of immune memory may have occurred after the first treatment injection. Given the time frame of our exploratory study and previous research on acquired antibody production timing in reptiles, we suggest that our observations may be products of immune training/priming, tolerance, and resource reallocation. However, more work is necessary to examine these processes in reptiles and we make suggestions for future research directions. Our work further demonstrates the role that diverse immunological tools have in understanding immune strategies across taxa to enhance our knowledge of reptilian immunology and inform conservation decisions. 
    more » « less